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Unraveling Adaptation of Pontibacter Korlensis to Radiation and Infertility

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Unraveling Adaptation of Pontibacter Korlensis to Radiation and Infertility www.nature.com/scientificreports OPEN Unraveling adaptation of Pontibacter korlensis to radiation and infertility in desert Received: 13 December 2014 Accepted: 27 April 2015 through complete genome and Published: 09 June 2015 comparative transcriptomic analysis Jun Dai1,*, Wenkui Dai2,*, Chuangzhao Qiu2,*, Zhenyu Yang2, Yi Zhang1, Mengzhou Zhou1, Lei Zhang3, Chengxiang Fang4, Qiang Gao2, Qiao Yang5, Xin Li1, Zhi Wang1, Zhiyong Wang6, Zhenhua Jia1 & Xiong Chen1 The desert is a harsh habitat for flora and microbial life due to its aridness and strong radiation. In this study, we constructed the first complete and deeply annotated genome of the genus Pontibacter (Pontibacter korlensis X14-1T = CCTCC AB 206081T, X14-1). Reconstruction of the sugar metabolism process indicated that strain X14-1 can utilize diverse sugars, including cellulose, starch and sucrose; this result is consistent with previous experiments. Strain X14-1 is also able to resist desiccation and radiation in the desert through well-armed systems related to DNA repair, radical oxygen species (ROS) detoxification and the OstAB and TreYZ pathways for trehalose synthesis. A comparative transcriptomic analysis under gamma radiation revealed that strain X14-1 presents high-efficacy operating responses to radiation, including the robust expression of catalase and the manganese transport protein. Evaluation of 73 novel genes that are differentially expressed showed that some of these genes may contribute to the strain’s adaptation to radiation and desiccation through ferric transport and preservation. Approximately 10% of the Earth’s terrestrial surface is covered by desert with arid environments, which are characterized as environments with nutrient limitation, desiccation, cycles of extreme temperatures and intense radiation1. Nevertheless, diverse bacterial species have been identified and isolated from this extreme biotope2–5 and have been found to be tolerant to solar radiation through various mechanisms, such as DNA repair, ROS detoxification and protein protection6. Since the radiation-resistant strain Deinococcus radiodurans R1 was isolated 50 years ago, stud- ies of bacterial resistance and tolerance to solar radiation have been mainly performed on the genus Deinococcus7. D. radiodurans is 200-fold and 20-fold more resistant to ionizing radiation and UV 1Key Laboratory of Fermentation Engineering (Ministry of Education), Hubei Provincial Cooperative Innovation Center of Industrial Fermentation, College of Bioengineering, Hubei University of Technology, Wuhan 430068, China. 2BGI Shenzhen, Shenzhen 518083, China. 3College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, China. 4China Center for Type Culture Collection (CCTCC), College of Life Sciences, Wuhan University, Wuhan 430072, China. 5East China Sea fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai 200090, China. 6BGI Yunnan, Kunming 650228, China. *These authors contributed equally to this work. Correspondence and requests for materials should be addressed to X.C. (email: [email protected]) SCIENTIFIC REPORTS | 5:10929 | DOI: 10.1038/srep10929 1 www.nature.com/scientificreports/ P. korlensis Pontibacter P. ros e u s X14-1 P. actiniarum DSM19842 sp. BAB1700 DSM17521 Habitat Desert Aquatic Multiple NA Genome size(Mb) 5.46 4.95 4.54 4.58 GC content(%) 47.3 53.1 50.0 52.6 Total genes 5,037 4,689 4,849 4,260 Coding regions(%) 86.58 86.42 84.97 87.01 Unannotated genes 893 901 507 328 Insertion sequence 4 6 1 0 Prophage 1 0 0 0 Transposase/Integrase 114 28 10 5 Table 1. Comparison of strain X14-1 with other species in genus Pontibacter. irradiation, respectively, than Escherichia coli8, and the complete genome of D. radiodurans was first published in 19999. To elucidate the extreme resistance phenotype of D. radiodurans R1, various research strategies have been combined10, and three hypotheses regarding DNA repair have been proposed11. The lack of novelty in DNA repair-related genes/proteins and the greater efficiency of specific bacteria to use conventional repair pathways are partially supported by the findings from previous studies12–17. An in-depth analysis of the D. radiodurans R1 genome and its gene expression profile revealed that many undefined genes, including ddrA, ddrB, ddrC, ddrD and pprA, are involved in DNA repair18–21, suggest- ing that repair functions are encoded by these hypothetical genes. The last hypothesis is that ring-like nucleoids (RNs) contribute to DNA repair22. There are also three assumptions regarding the maintenance of a low ROS concentration in bacte- ria10, most of which are detoxifying and scavenging ROS, including small catalase, superoxide dismu- tase, and antioxidant molecules, and exhibit an increased Mn(II)/Fe ratio intermediated by manganese complexes11,13,23. Daly and Krisko found that molecules smaller than 3 kDa in the extract of Deinococcus radiodurans R1 can impose antioxidant protection on E. coli proteins23,24. The promotion of metabolic activities with decreased ROS production (e.g., glyoxylate bypass of the TCA cycle21,25) is an alternative to the response to oxidative damage and single antioxidant pathways through high ROS production, which could be inactivated due to redundant ROS-tolerance mechanisms. To lower the ROS, it is also helpful to reduce proteins with Fe-S clusters and the number of respiratory chain enzymes25. In addition to maintaining a low ROS concentration, many other metabolic activities, such as proteolysis and glucose metabolism, contribute to the robustness of D. radiodurans R115,23,26,27. In addition to D. radiodurans R1, additional genome sequences of the genus Deinococcus have been published26,28–32, and comparative anal- yses have been performed to elucidate the diverse molecular mechanisms and physiological determinants underlying the extreme resistance phenotype33,34. We isolated the strain Pontibacter korlensis X14-1T (X14-1) from the surface layer of a desert in Xinjiang, China, and identified it as a new species of the genus Pontibacter2. This study provides the first complete genome of the genus Pontibacter and attempted to delineate genomic components related to radiation and desiccation resistance in comparison with other species from the genus Pontibacter. A comparative analysis of the gene expression profile under radiation was also conducted to unravel the complicated mechanisms of strain X14-1 involved in its adaptation to the arid environment of the desert. This work will provide referable information for the comprehensive understanding of the evolution and adaptation of the genus Pontibacter as well as various radiation and desiccation resistances. Results Genomic characteristics and phylogeny of strain X14-1. The complete genome sequence of strain X14-1 was produced based on high-quality reads and corrected by read mapping and PCR ver- ification. Strain X14-1 has a larger genome size (5.46 MB) and a lower GC content (47.3%) than three other Pontibacter strains distributed in different species (summarized in Table 1). We found that most of the transposase-related genes are located near genomic islands and next to DNA repair- and ROS detoxification-related genes (Fig. 1), which implied that mobile genetic elements (MGEs) play an impor- tant role in the adaptation to radiation and desiccation in the desert. Differences in genome size and MGEs between strain X14-1 and other Pontibacter strains may be attributed to the genomic evolution or gapped assembly of P. actiniarum DSM 19842, Pontibacter sp. BAB1700 and P. roseus DSM 17521. To confirm the phylotype of strain X14-1, we downloaded 40 genomes of the family Cytophagaceae (higher taxonomic classification of the genus Pontibacter) available in the NCBI database. Phylogeny analysis indicated the same results as those previously reported based on the 16S rDNA sequence2, and P. actiniarum DSM 19842 was found to be the most homologous to strain X14-1 (Fig. 2), a finding that is also supported by the following functional analysis. SCIENTIFIC REPORTS | 5:10929 | DOI: 10.1038/srep10929 2 www.nature.com/scientificreports/ Figure 1. Genomic components of P. korlensis X14-1. Distribution of genes, genomic islands, transposases, DNA repair and oxidative response related determinants in the genome of strain X14-1. It indicates that strain X14-1 harbors abundant MGEs, suggestive of high genome plasticity. Sugar metabolism in strain X14-1. In comparison with three other genomes from the genus Pontibacter, we found that only strain X14-1 harbors genes encoding D-fructokinase, which is essen- tial for sucrose and fructose utilization, and this is consistent with previous experimental results2. Beta-galactosidase, which is essential for strain X14-1 to use lactose as an alternative carbon source by catalyzing lactose to galactose and glucose, is specific to strain X14-1 compared with other Pontibacter strains. Although comparative analysis revealed a common dispersion of cellobiose glucohydrolase in Pontibacter, enzymes responsible for degrading cellulose to cellobiose are only distributed in strain X14-1. Starch could be degraded to amylose and alpha-D-galactose-1-phosphate, which is an interme- diate in the production of UDP-glucose that could link pentose and glucuronate interconversion. This is important for the utilization of D-galactose as a carbon resource. Mannose can enter glycolysis through beta-D-fructose-6-phosphate with the help of hexokinase and mannose-6-phosphate isomerase, which could be encoded by genes in strain X14-1.
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